Suppression without inhibition: how retinal computation contributes to saccadic suppression

Visual perception remains stable across saccadic eye movements, despite the concurrent strongly disruptive visual flow. This stability is partially associated with a reduction in visual sensitivity, known as saccadic suppression, which already starts in the retina with reduced ganglion cell sensitivity. However, the retinal circuit mechanisms giving rise to such suppression remain unknown. Here, we describe these mechanisms using electrophysiology in mouse, pig, and macaque retina, 2-photon calcium imaging, computational modeling, and human psychophysics. We find that sequential stimuli, like those that naturally occur during saccades, trigger three independent suppressive mechanisms in the retina. The main mechanism is triggered by contrast-reversing sequential stimuli and originates within the receptive field center of ganglion cells. It does not involve inhibition or other known suppressive mechanisms like saturation or adaptation. Instead, it relies on temporal filtering of the inherently slow response of cone photoreceptors coupled with downstream nonlinearities. Two further mechanisms of suppression are present predominantly in ON ganglion cells and originate in the receptive field surround, highlighting another disparity between ON and OFF ganglion cells. The mechanisms uncovered here likely play a role in shaping the retinal output following eye movements and other natural viewing conditions where sequential stimulation is ubiquitous.


REVIEWERS' COMMENTS:
Reviewer #1 (Remarks to the Author): The manuscript by Idrees et al. has much improved and clarified. I only have some minor comments left.
The model of ganglion cell responses used to analyze the effects of model transiency and of the threshold in the nonlinearity is really difficult to parse. I would be helpful, for example, if examples of the filters could be shown. (E.g. for transiency parameter = 0, 0.5, 1 or something like this.) Also, why is the nonlinearity transiency parameter called this way? Does it relate to transiency? And maybe explain in the main text (around lines 455) in what sense it is made "more strict". I guess more strict corresponds to higher threshold?
In the Methods section, I was confused by the small time scales (mu=3ms, sigma=1ms), which should lead to very brief and rapidly oscillating filters, whereas In the new section on the apparent pre-saccadic suppression, I was wondering whether one should think of the response to non-preferred contrast as a response to the onset of the flash (thus relating to ON-OFF cells) or whether this is rather a rebound response to the offset of the flash. Maybe the authors want to at least mention these possibilities, as they may be important when considering potential mechanisms.
Responses to Reviewer Comments on: "Suppression without inhibition: How retinal computation contributes to saccadic suppression" Idrees, Baumann, Korympidou, Schubert, Kling, K Franke, Hafed, F Franke*, Münch* We thank the reviewer for their insightful comments to help finalize our manuscript.
In what follows, we provide specific responses to the reviewer comments (colored in blue text), which we have incorporated into the final version of this manuscript.
The manuscript by Idrees et al. has much improved and clarified. I only have some minor comments left.
We thank the reviewer for this encouraging remark.
The Also, why is the nonlinearity transiency parameter called this way? Does it relate to transiency? And maybe explain in the main text (around lines 455) in what sense it is made "more strict". I guess more strict corresponds to higher threshold? As pointed out by the reviewer, more strict indeed corresponds to higher threshold values. We have added this explanation in the main text (lines 451-454). We have also simplified the terminology by calling it a thresholding nonlinearity. Similarly, the filter transiency parameter is now referred to as the filter transiency.
In the Methods section, I was confused by the small time scales (mu=3ms, sigma=1ms), which should lead to very brief and rapidly oscillating filters, whereas We are comparing the rate of change in cone output of a flash presented immediately after a luminance step with a flash presented long after the luminance step. We have edited the text to make this comparison explicit (lines 423-426) In comparison to preferred contrast flashes, the responses to non-preferred contrast have a much higher latency with respect to both the onset and offset of the flash. The origins, mechanisms and the role of these delayed responses are not well studied, which we explicitly state in lines 658-662.